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Studies in humans

Intra-uterine exposure to lower maternal haemoglobin concentration is associated with impaired cognitive function in stunted adolescents: results from a 17-year longitudinal cohort study in Indonesia

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Pages 826-835 | Received 04 Jul 2023, Accepted 02 Oct 2023, Published online: 11 Oct 2023

References

  • Agustina R, Nadiya K, El Andini A, Setianingsih AA, Sadariskar AA, Prafiantini E, Wirawan F, Karyadi E, Raut MK. 2020. Associations of meal patterning, dietary quality and diversity with anemia and overweight-obesity among Indonesian schoolgoing adolescent girls in West Java. PLoS One. 15(4):e0231519. doi: 10.1371/journal.pone.0231519.
  • Alam MA, Richard SA, Fahim SM, Mahfuz M, Nahar B, Das S, Shrestha B, Koshy B, Mduma E, Seidman JC, et al. 2020. Impact of early-onset persistent stunting on cognitive development at 5 years of age: results from a multi-country cohort study. PLoS One. 15(2):e0229663. doi: 10.1371/journal.pone.0229663.
  • Alwan N, Hamamy H. 2015. Maternal iron status in pregnancy and long-term health outcomes in the offspring. J Pediatr Genet. 4(2):111–123. doi: 10.1055/s-0035-1556742.
  • Aranda N, Hernández-Martínez C, Arija V, Ribot B, Canals J. 2017. Haemoconcentration risk at the end of pregnancy: effects on neonatal behaviour. Public Health Nutr. 20(8):1405–1413. doi: 10.1017/S136898001600358X.
  • Barkley JS, Kendrick KL, Codling K, Muslimatun S, Pachón H. 2015. Anaemia prevalence over time in Indonesia: estimates from the 1997, 2000, and 2008 Indonesia Family Life Surveys. Asia Pac J Clin Nutr. 24(3):452–455.
  • Beard JL. 2008. Why iron deficiency is important in infant development. In. J Nutr. 138(12):2534–2536. doi: 10.1093/jn/138.12.2534.
  • Beard JL, Felt B, Schallert T, Burhans M, Connor JR, Georgieff MK. 2006. Moderate iron deficiency in infancy: biology and behavior in young rats. Behav Brain Res. 170(2):224–232. doi: 10.1016/j.bbr.2006.02.024.
  • de Benoist B, McLean E, Egli I, Cogswell M. 2008. Worldwide prevalence on anaemia 1993-2005. Geneva: WHO.
  • Black MM, Walker SP, Fernald LCH, Andersen CT, DiGirolamo AM, Lu C, McCoy DC, Fink G, Shawar YR, Shiffman J, et al. 2017. Early childhood development coming of age: science through the life course. Lancet. 389(10064):77–90. doi: 10.1016/S0140-6736(16)31389-7.
  • Carter RC, Jacobson JL, Burden MJ, Armony-Sivan R, Dodge NC, Angelilli ML, Lozoff B, Jacobson SW. 2010. Iron deficiency anemia and cognitive function in infancy. Pediatrics. 126(2):e427–434. doi: 10.1542/peds.2009-2097.
  • Chandra AF, Marsigit J, Pratiwi AA, Akhmad SR, Andrianus A, Priyatini T. 2018. Education and socioeconomic status as risk factors of anemia in pregnancy: a cross-sectional study in Puskesmas Kecamatan Duren Sawit. Adv Sci Lett. 24(9):6526–6529. doi: 10.1166/asl.2018.12765.
  • Chang S, Zeng L, Brouwer ID, Kok FJ, Yan H. 2013. Effect of iron deficiency anemia in pregnancy on child mental development in rural China. Pediatrics. 131(3):e755–e763. doi: 10.1542/peds.2011-3513.
  • Chaparro CM, Suchdev PS. 2019. Anemia epidemiology, pathophysiology, and etiology in low- and middle-income countries. Ann N Y Acad Sci. 1450(1):15–31. doi: 10.1111/nyas.14092.
  • Christian P, Smith ER. 2018. Adolescent undernutrition: global burden, physiology, and nutritional risks. Ann Nutr Metab. 72(4):316–328. doi: 10.1159/000488865.
  • Crookston BT, Forste R, McClellan C, Georgiadis A, Heaton TB. 2014. Factors associated with cognitive achievement in late childhood and adolescence: the Young Lives cohort study of children in Ethiopia, India, Peru, and Vietnam. BMC Pediatr. 14(1):253. doi: 10.1186/1471-2431-14-253.
  • Danaei G, Andrews KG, Sudfeld CR, Fink G, McCoy DC, Peet E, Sania A, Smith Fawzi MC, Ezzati M, Fawzi WW. 2016. Risk factors for childhood stunting in 137 developing countries: a comparative risk assessment analysis at global, regional, and country levels. PLoS Med. 13(11):e1002164. doi: 10.1371/journal.pmed.1002164.
  • Fararouei M, Robertson C, Whittaker J, Sovio U, Ruokonen A, Pouta A, Hartikainen AL, Jarvelin MR, Hyppönen E. 2010. Maternal Hb during pregnancy and offspring’s educational achievement: a prospective cohort study over 30 years. Br J Nutr. 104(9):1363–1368. doi: 10.1017/S0007114510002175.
  • Fiedler J, D’Agostino A, Sununtnasuk C. 2014. Technical brief a rapid initial assessment of the distribution and consumption of iron – folic acid tablets through antenatal care in Ethiopia. Arlington (VA): USAID/Strengthening Partnerships, Results, and Innovations in Nutrition Globally (SPRING) Project.
  • Frankenberg E, Thomas D. 2000. The Indonesia Family Life Survey (IFLS): study design and results from waves 1 and 2. DRU-2238/1-NIA/NICHD.
  • Fretham SJB, Carlson ES, Georgieff MK. 2011. The role of iron in learning and memory. Adv Nutr. 2(2):112–121. doi: 10.3945/an.110.000190.
  • Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL. 1999. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci. 2(10):861–863. doi: 10.1038/13158.
  • Grantham-McGregor S, Ani C. 2001. A review of studies on the effect of iron deficiency on cognitive development in children. J Nutr. 131(2S-2):649S–668S. doi: 10.1093/jn/131.2.649S.
  • Hanifah L, Wulansari R, Meiandayati R, Achadi EL. 2018. Stunting trends and associated factors among Indonesian children aged 0-23 months: evidence from Indonesian Family Life Surveys (IFLS) 2000, 2007 and 2014. Malays J Nutr. 24(3):315–322.
  • Hernández-Martínez C, Canals J, Aranda N, Ribot B, Escribano J, Arija V. 2011. Effects of iron deficiency on neonatal behavior at different stages of pregnancy. Early Hum Dev. 87(3):165–169. doi: 10.1016/j.earlhumdev.2010.12.006.
  • Irianti S, Prasetyoputra P. 2021. Rural–urban disparities in access to improved sanitation in indonesia: a decomposition approach. SAGE Open. 11(3):215824402110299. doi: 10.1177/21582440211029920.
  • Janbek J, Sarki M, Specht IO, Heitmann BL. 2019. A systematic literature review of the relation between iron status/anemia in pregnancy and offspring neurodevelopment. Eur J Clin Nutr. 73(12):1561–1578. doi: 10.1038/s41430-019-0400-6.
  • Kementerian Kesehatan Republik Indonesia. 2018. Laporan Nasional Riset Kesehatan Dasar 2018 (Report of Indonesian Basic Health Survey 2018). Kementerian Kesehatan Republik Indonesia. http://labdata.litbang.kemkes.go.id/images/download/laporan/RKD/2018/Laporan_Nasional_RKD2018_FINAL.pdf.
  • Kozuki N, Lee AC, Katz J. 2012. Moderate to severe, but not mild, maternal anemia is associated with increased risk of small-for-gestational-age outcomes. J Nutr. 142(2):358–362. doi: 10.3945/jn.111.149237.
  • Lozoff B, Beard J, Connor J, Felt B, Georgieff M, Schallert T. 2006. Long-lasting neural and behavioral effects of iron deficiency in infancy. Nutr Rev. 64(5 Pt 2):S34–S43. doi: 10.1301/nr.2006.may.s34-s43.
  • Maika A, Mittinty MN, Brinkman S, Lynch J. 2015. Effect on child cognitive function of increasing household expenditure in Indonesia: application of a marginal structural model and simulation of a cash transfer programme. Int J Epidemiol. 44(1):218–228. doi: 10.1093/ije/dyu264.
  • Mehmetoglu M. 2018. Medsem: a Stata package for statistical mediation analysis. Int J Comput Econ Econom. 8(1):63–78.
  • Mendez MA, Adair LS. 1999. Severity and timing of stunting in the first two years of life affect performance on cognitive tests in late childhood. J Nutr. 129(8):1555–1562. doi: 10.1093/jn/129.8.1555.
  • Menon KC, Ferguson EL, Thomson CD, Gray AR, Zodpey S, Saraf A, Das PK, Skeaff SA. 2016. Effects of anemia at different stages of gestation on infant outcomes. Nutrition. 32(1):61–65. doi: 10.1016/j.nut.2015.07.009.
  • Mireku MO, Davidson LL, Koura GK, Ouédraogo S, Boivin MJ, Xiong X, Accrombessi MMK, Massougbodji A, Cot M, Bodeau-Livinec F. 2015. Prenatal hemoglobin levels and early cognitive and motor functions of one-year-old children. Pediatrics. 136(1):e76–e83. doi: 10.1542/peds.2015-0491.
  • Motta RW, Joseph JM. 2000. Group intelligence tests. In Goldstein, G. (2008). Intellectual evaluation. In: Hersen M, Gross AM, editors. Handbook of clinical psychology. Vol. 1. Hoboken (NJ): Wiley; p. 395–421.
  • Nair M, Choudhury MK, Choudhury SS, Kakoty SD, Sarma UC, Webster P, Knight M. 2016. Association between maternal anaemia and pregnancy outcomes: a cohort study in Assam, India. BMJ Glob Heal. 1(1):1–9.
  • O’Shea A, Cohen RA, Porges EC, Nissim NR, Woods AJ. 2016. Cognitive aging and the hippocampus in older adults. Front Aging Neurosci. 8:298. doi: 10.3389/fnagi.2016.00298.
  • Prabhakaran V, Smith JAL, Desmond JE, Glover GH, Gabrieli JDE. 1997. Neural substrates of fluid reasoning: an fMRI study of neocortical activation during performance of the Raven’s Progressive Matrices Test. Cogn Psychol. 33(1):43–63. doi: 10.1006/cogp.1997.0659.
  • Prado EL, Sebayang SK, Apriatni M, Adawiyah SR, Hidayati N, Islamiyah A, Siddiq S, Harefa B, Lum J, Alcock KJ, et al. 2017. Maternal multiple micronutrient supplementation and other biomedical and socioenvironmental influences on children’s cognition at age 9–12 years in Indonesia: follow-up of the SUMMIT randomised trial. Lancet Glob Health. 5(2):e217–e228. doi: 10.1016/S2214-109X(16)30354-0.
  • Preedy VR. 2012. Handbook of anthropometry: physical measures of human form in health and disease. Cham: Springer; p. 1–3107.
  • Rahman MM, Abe SK, Rahman MS, Kanda M, Narita S, Bilano V, Ota E, Gilmour S, Shibuya K. 2016. Maternal anemia and risk of adverse birth and health outcomes in low- and middle-income countries: systematic review and meta-analysis. Am J Clin Nutr. 103(2):495–504. doi: 10.3945/ajcn.115.107896.
  • Rahman MS, Mushfiquee M, Masud MS, Howlader T. 2019. Association between malnutrition and anemia in under-five children and women of reproductive age: evidence from Bangladesh demographic and Health Survey 2011. PLoS One. 14(7):e0219170. doi: 10.1371/journal.pone.0219170.
  • Raven J. 2000. The Raven’s progressive matrices: change and stability over culture and time. Cogn Psychol. 41(1):1–48. doi: 10.1006/cogp.1999.0735.
  • Rizky M, Suryadarma D, Suryahadi A. 2019. Effect of growing up poor on labor market outcomes. ADBI Work Pap Ser. Asian Development Bank Institute. Available from: https://www.adb.org/sites/default/files/publication/526866/adbi-wp1002.pdf.
  • Sandjaja S, Poh BK, Rojroonwasinkul N, Le Nyugen BK, Budiman B, Ng LO, Soonthorndhada K, Xuyen HT, Deurenberg P, Parikh P. 2013. Relationship between anthropometric indicators and cognitive performance in Southeast Asian school-aged children. Br J Nutr. 110 Suppl 3(S3):S57–S64. doi: 10.1017/S0007114513002079.
  • Sania A, Sudfeld CR, Danaei G, Fink G, McCoy DC, Zhu Z, Fawzi MCS, Akman M, Arifeen SE, Barros AJD, et al. 2019. Early life risk factors of motor, cognitive and language development: A pooled analysis of studies from low/middle-income countries. BMJ Open. 9(10):e026449. doi: 10.1136/bmjopen-2018-026449.
  • Sartika RAD, Fajarini IA, Fitrianing L. 2019. Relationship between expenditures for food purchasing and adolescent anemia in Indonesia. Pak J Nutr. 18(2):171–177. doi: 10.3923/pjn.2019.171.177.
  • StataCorp. 2019. Stata Statistical Software: release 16. College Station (TX): StataCorp LLC.
  • Strauss J, Witoelar F, Sikoki B. 2016. The Fifth Wave of the Indonesia Family Life Survey: overview and field report: volume 1. March 2016. WR-1143/1-NIA/NICHD.
  • Sungthong R, Mo-Suwan L, Chongsuvivatwong V. 2002. Effects of haemoglobin and serum ferritin on cognitive function in school children. Asia Pac J Clin Nutr. 11(2):117–122. doi: 10.1046/j.1440-6047.2002.00272.x.
  • The World Bank. 2017. Improving education quality in Indonesia’s poor rural and remote areas. WB. Available from: https://www.worldbank.org/en/results/2017/12/22/improving-education-quality-in-indonesia-poor-rural-and-remote-areas.
  • Todorich B, Pasquini JM, Garcia CI, Paez PM, Connor JR. 2009. Oligodendrocytes and myelination: the role of iron. Glia. 57(5):467–478. doi: 10.1002/glia.20784.
  • Tran TD, Tran T, Simpson JA, Tran HT, Nguyen TT, Hanieh S, Dwyer T, Biggs BA, Fisher J. 2014. Infant motor development in rural Vietnam and intrauterine exposures to anaemia, iron deficiency and common mental disorders: a prospective community-based study. BMC Pregnancy Childbirth. 14(1):8. doi: 10.1186/1471-2393-14-8.
  • Vaezghasemi M, Razak F, Ng N, Subramanian SV. 2016. Inter-individual inequality in BMI: an analysis of Indonesian Family Life Surveys (1993–2007). SSM Popul Health. 2:876–888. doi: 10.1016/j.ssmph.2016.09.013.
  • Veena SR, Gale CR, Krishnaveni GV, Kehoe SH, Srinivasan K, Fall CHD. 2016. Association between maternal nutritional status in pregnancy and offspring cognitive function during childhood and adolescence; a systematic review. BMC Pregnancy Childbirth. 16(1):220. doi: 10.1186/s12884-016-1011-z.
  • Walker SP, Chang SM, Powell CA, Grantham-McGregor SM. 2005. Effects of early childhood psychosocial stimulation and nutritional supplementation on cognition and education in growth-stunted Jamaican children: prospective cohort study. Lancet. 366(9499):1804–1807. doi: 10.1016/S0140-6736(05)67574-5.
  • Wang JY, Hu PJ, Luo DM, Dong B, Ma Y, Dai J, Song Y, Ma J, Lau PWC. 2020. Reducing anemia among school-aged children in china by eliminating the geographic disparity and ameliorating stunting: evidence from a national survey. Front Pediatr. 8:193. doi: 10.3389/fped.2020.00193.
  • Witoelar F. 2009. Note on the construction of the IFLS consumption expenditure aggregates. Available from: https://dokumen.tips/documents/ifls-consumption-expendi%0Dture-aggregatespdf.html.
  • World Health Organization. 2007. Growth reference data for 5-19 years. WHO. Available from: https://www.who.int/tools/growth-reference-data-for-5to19-years.
  • World Health Organization. 2011. The global prevalence of anaemia in 2011. WHO. Available from: https://apps.who.int/iris/bitstream/handle/10665/177094/9789241564960_eng.pdf.
  • World Health Organization. 2013. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Vitamin and Mineral Nutrition Information System. WHO. Available from: https://www.who.int/publications/i/item/WHO-NMH-NHD-MNM-11.1.